The always fascinating Aeon Magazine has a very interesting piece up by my friend David Dobbs, Die, selfish gene, die. As you can tell it is something of a broadside against Richard Dawkins’ ideas promoted in The Selfish Gene. The subheading is straightforward: “The selfish gene is one of the most successful science metaphors ever invented. Unfortunately, it’s wrong.” As I stated on Twitter the writing here was splendid, but at the end of the day I must disagree with the conclusions on the balance. It is true that the selfish gene is wrong as a metaphor and model, but all representations of this sort have an element of stylized artifice which does not stand up to scrutiny. John Dalton’s atomic theory is also wrong, but still highly useful in imparting conceptual truth. But across 5,000 words David surveys the landscape and seems to come away with the lesson that evolutionary biology took a wrong turn at some point, and that the calcified old order is now facing a revolt from below. To me this does not seem like an accurate representation of what I know, though to be fair sometimes it was difficult for me to gauge whether David himself is always of one mind on the issue. The piece is wide ranging and expansive, and has so much detail that it is difficult to start at one particular place.

Naturally I have some technical and scientific gripes which may be irrelevant to most readers. As I observed on Twitter the mention of microarrays as a means to understand gene expression makes me wonder if this piece was written in 2005, as the field has moved to RNA-Seq. David admitted that this article was years in the making, so this peculiarity is easily explained then. But there is another section where he characterizes William D. Hamilton as a statistician. I think this misleads somewhat as to the primary thrust of his career. To my knowledge Hamilton’s forte was not detailed analysis of reams of data, extracting patterns from the noise. Rather, he engaged in modeling, extrapolating from the core truths of Mendelian genetics.

But the above are minor gripes, and more matters of style than substance. There are some issues where I think the piece may be substantively incorrect. Going in order of my concern, first David seems to imply that the genius of genetics in relation to Charles Darwin’s theory of natural selection is that it presented a straightforward mechanism by which one could introduce variation through mutation. This seems wrong to me. Rather, the power of genetics in a Mendelian framework is that it is a discrete manner of transmission where variation does not decay every generation. Natural selection needs variation to operate, and previous “blending models” of inheritance were subject to the problem that variation decays very rapidly in this framework. Second, the piece contends that the modern evolutionary synthesis was “all about the maths.” A formal mathematical framework was probably a necessary condition for the synthesis as we understand it, but it seems too much to say that this was overwhelmingly dominant. Two of the major figures in the synthesis, Theodosius Dobzhansky and Ernst Mayr, were definitely not mathematical. Dobzhansky saw particular empirical results, and leaned upon Sewall Wright’s formal models to support them, but he admitted that the mathematics escaped him. Mayr famously inveighed against mathematical genetics in his later years.

Then there’s the description of the origin and development of the theory of inclusive fitness. This just seems totally wrong to me (unless it is simply not clear). Though both R. A. Fisher and J. B. S. Haldane alluded to the broader logic of inclusive fitness at various points, the mathematical framework was developed by William D. Hamilton, John Maynard Smith, and George Price in the 1960s. More precisely, two papers in 1964 by Hamilton titled The Genetical Evolution of Social Behaviour laid the groundwork for the formal exploration of the problem of altruism. If I had read the piece without that knowledge I’d have thought it had been developed decades earlier.

Reading through the article I could almost see areas that I felt had to be edited out, or rewritten to be comprehensible to the broader public. I admire David’s effort and doubt I could have pulled something similar off. This is not an easy topic to tackle, the conceptual and empirical landscape is a minefield for someone to explore. Too many of the scientific assertions in the detail I’m not sure I can respond to, because I’m not totally clear on what’s being said, or implied. Many complex ideas and positions are condensed down to a sentence or two, to the point where they become obscure to me.

But there are a few points I’d like to enter into the record. First, as noted by many ideas like genetic assimilation have been around for a long time.C. H. Waddington is not an obscure figure. Evolutionary genetics has not been in stasis since the modern synthesis, or even the 1970s. Genomics means that there is a surfeit of data, and different theories are going to be useful in explaining particular aspects of the shape of biological variation. The emergence of evo-devo in the 2000s was certainly interesting, though I don’t think it “changed everything,” as some are fond of declaring. The narrative that the modern synthesis is being “overthrown” seems to be a persistent one, and always seems t finds support from the latest hot area of study. In the 1970s it was the molecular theory of neutral evolution, which rebutted excessive adaptationism, in the 2000s it was evo-devo, and now it is epigenetics. Science is not like religion, and heretical sects do not just explode and extinguish. New methods and areas of study add and modify the consensus, but only in rare cases do they “overthrow” a paradigm. The current interest in epigenetic inheritance has spawned forth a craze in neo-Lamarckian headlines. This too shall pass.

Finally, there’s the namecheck of several biologists who are presenting an alternative to ‘selfish gene’ model, Massimo Pigliucci, Eva Jablonka, Stuart Kauffman, Stuart A Newman, Stephen Jay Gould, Gregory Wray and Mary Jane West-Eberhard. To the lay reader some of these are familiar names already. It seems that citing them is a way to bolster the case that it isn’t crazy to think that Richard Dawkins’ ideas may not be right. These aren’t all cranks. But, some of them are notable for being heterodox in their thinking. Which leads me to assert that Richard Dawkins’ views are still closer to the center of opinions among evolutionary biologists than Mary Jane West-Eberhard. That doesn’t mean that Dawkins is right and West-Eberhard is wrong, it just means implicitly ‘gene-centric’ models are still popular. There’s a reason it’s calle ‘genetics,’ and not ‘expressionetics.’

I could say much more, but I won’t. After thrashing David a fair amount I have to admit it was a pleasure to read a popular piece which cited the achievements of greats like Fisher, Haldane, Wright, and Hamilton. Though I’d warn you from taking the assertions as gospel, the article is still worth reading for its detail as a starting point for further exploration.

I had just finished reading the essay by David Dobbs when your review of it came to my attention. I like most of what you say here, and it is very nuanced. You don’t beat around the bush too much before you get to the point that you still think the gene-centric view promoted by Richard Dawkins represents the current orthodoxy. You present this as if it were an intellectual fortress against which waves of faddish thinking by lesser intellects will not only break, but be broken.

I am not so sure about this particular “fad”. True, epigenetic adaptation, to some people who want a catchy headline, implies that Lamarkian ideas are not so “crazy” after all. But I seriously doubt if that is what excited Pigliucci or Mary Jane… on the contrary, it is the idea that a gene might not just BE a gene, but many different genes, depending on the set of instructions for reading it. We’ve known for a long time that genes can be turned on or off. We’ve also known that there is even a diurnal cycle to this, which varies by organ system. Now we find out that they can be read differently, depending upon the key code (as it were) entered.

So yes, Dawkins is right – it still comes down to the gene in the end. That is the final replicant that is selection’s “target”. However we have now learned there are some wrinkles, in addition to the sheer number, of layers of phenotypical reality through which natural selection must delve to hit that target.

Wrinkles may seem more significant to me, than to you, given out respective ages. To me, frankly, I begin to wonder if the effects of natural selection might sometimes miss the target altogether, given enough wrinkles. It might actually wind up selecting for certain wrinkles, not certain individual genes.

If the wrinkles are behavioural adaptations, particularly ones which alter gene expression in ways that deflect the arrow of causality between an environmental challenge and an individual’s survival and reproductive success, that changes the paradigm. Depending upon which behavioural tradition an individual is born into, their possession of a particular gene may matter less, or more.

Okay, let us back away format he dangerous ground. Let’s look at bacteria and not multicellular organisms in groups and all the potential wrinkles we might find there. It turns out, there are even epigenetic processes working within the lives of bacteria. Quorum sensing has been extensively studied in bacteria: as inter-cell communication between individual bacteria increase within an environment, or if a threatening toxin is sensed, bacteria will “switch on” the genes that induce colony formation and the production of immunity enhancing biofilms. See http://link.springer.com/article/10.1186%2F1745-6150-4-6#page-1 and especially this recent paper http://rsbl.royalsocietypublishing.org/content/9/5/20130548.full.

And this has something interesting to say about the benefits to the cooperative individuals and the “cheaters” – the cooperative bacteria that respond to threats through the quorum sensitive mechanism tend to reproduce better than the “cheater” bacteria that do not cooperate in this biofilm production but are also protected by it.

Imagine the implications of this. Here it gets interesting, doesn’t it? As quoted from the final cited example:

“Mutations in QS genes reduce biofilm strength [14,15], and while cheats can invade biofilms [13], growth within an aggregation will, by definition, spatially structure the population, increasing the probability of cooperators being spatially associated with other cooperators. Crucially, being in a large cell aggregation has been shown to increase resistance against predation by ciliate protists [16,17]. We found here that cheat biofilms were more vulnerable to predation by protists yielding higher protist cell numbers, whereas cooperators formed larger and denser cell aggregations in the liquid phase of the culture medium. We therefore suggest that wild-type bacteria were more resistant because they could produce and respond to QS signals in biofilms, resulting in larger and stronger cell aggregations. Cheats were presumably unable to exploit these aggregations because of population structure: biofilm growth mode could exclusively favour cooperators by increasing relatedness [18]. Alternatively, biofilms containing both the wild-type and cheat could have been less resistant, and thus more readily consumed by protists [13]. In the case of signal-blind (lasR) mutants, it is also possible that their inability to QS even in the presence of wild-type bacteria made them individually more vulnerable to predation even when associated with an aggregation. Unfortunately, directly assessing the importance of cell aggregations to resistance is extremely difficult: P. aeruginosa forms aggregations even in constantly disturbed environments (shaken tubes [18]) making it hard to find a biofilm-free control environment.

In summary, our results demonstrate that trophic interactions, for instance predation, can affect the evolution of social interactions within species, potentially affecting the evolution of QS-signalling-regulated P. aeruginosa virulence in aquatic environmental reservoirs poor in nutrients.”

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the main issue is one of emphases. a lot of the things david brought up are well known/studied/of interest. but very few are claiming that they’re revolutions against the dominant paradigm. e.g., someone like sean carroll is not atypical. he is studies evo-devo, but doesn’t say that it’s some grand revolution that’s overthrowing an orthodoxy. someone like stephen jay gould did claim revolutionary insights. but someone like him is in the minority.

Great points. In addition to the historical errors, Dobbs seems to miss the basic point that those genotypes with the capacity to respond to environmental change do so via alleles that enable a greater response relative to other individuals in the population. So yes, there is no revolution, but rather a misunderstanding of the genetics of plasticity. Everyone that read the Dobbs article should read Lande in lieu of West-Eberhard (e.g., http://www.ncbi.nlm.nih.gov/pubmed/19467134). His mathematical treatment of this topic (starting in the 80′s) is clear and free of the hidden assumptions in the verbal arguments that get all of the press. All of this said, I agree that Dobbs is usually quite good.

The incorporation of non-nucleic heritable information into genetics seems like a pretty big deal – since it includes cultural variation, non-random mutations and intelligent design.

Of course you could argue that this revolution is not part of genetics – in which case there’s a revolution in memetics – or thereabouts – going on. However you look at it, it’s a pretty big shift for most evolutionary biologists.

I fear that you are too kind. Your account of Dobbs’ piece, critical though it is, gives it more credit than it is due (though I honour you for generosity towards a friend). As others note, genes matter since they are the unit of inheritance. All the phenotypic plasticity in the world doesn’t alter that. Nor does genetic assimilation — a much discussed, but rarely seen, phenomenon that is entirely compatible with ordinary genic selectionism. Epigenetics? In development, yes; cancer, yes; a few inherited pathologies too. But can anyone point to an adaptive trait in any organism encoded by an epigenetic modification rather than a good-old fashioned mutation? I seem to remember a paper by Enrico Coen on Antirrhinum. Yes, here it is: http://www.nature.com/nature/journal/v401/n6749/abs/401157a0.html. Nice — but a quick scan through the 500 odd citations suggests a dearth of similar examples. Evo-Devologists are identifying the molecular basis of adaptations. They map them and find…genes. (Tim Tyler, however, is right — culture, human culture, is special.) Dobbs’ article, which is of a familiar genre, aims to confuse rather than enlighten. And I truly dislike the conspiracy theory tone of it. But I venture that I am telling you nothing that you do not know.

So: cultural evolution has transformed the planet dramatically in the last few thousand years. Cultural variation is persistent enough to last for many thousands of years – in the case of bibles and hieroglyphics. Cultural variation is also widespread among non-human animals – with mating preferences being transmitted via social learning in organisms as lowly as fruit flies. I don’t really see how is this not a big deal. Cultural inheritance is a big deal. John Maynard Smith and Eörs Szathmáry identified it as one of the major transitions in evolution. The topic was hardly understood at all forty years ago. It has been a revolution.

TT, what are you talking about? maynard smith is one of the great men of evolutionary biology. dawkins invented meme. that issue, of cultural evolution, is a separate one from that focusing on biology separate from behavior.

Your title says “no revolution in genetics” – but there is an ongoing revolution in genetics, since it must incorporate directed mutations, inductive inference and intelligent design in order to deal with cultural evolution – and that is significant update for it. I’m trying to understand how you reconcile these things. Do you think that is not to do with genetics – and is a “separate” issue? If so, to recap, genetics is defined as being the science of heredity in living systems. Understanding how culture varies and recombines is part of its remit – because cultural variation is inherited in many types of living system.

[…] I’m often reluctant to get involved in online debates over the philosophy of biology as they usually shed more heat than light. That said, I’m going to do something stupid and comment on David Dobbs’ recent Aeon article “Die, selfish gene, die”. I’ve waited to comment in part because Dobbs’ article has a very different historical perspective (one that I think contains errors) from mine. I was glad to read that Razib Khan also thought that Waddington’s ideas about canalization and genetic assimilation are not in any way new. […]

[…] up evolution, part I and David Dobbs mucks up evolution, part II by jerry coyne – see also There is no revolution in genetics and Evolutionary orthodoxy may be boring, but it is probably true by razib – see also Science […]